MARINE ECOLOGY PROGRESS SERIES Vol. 165: 137-144,1998 Published May 7 Mar Ecol Prog Ser l

Behavioural responses to chemical cues of predation risk in a three-trophic-level Baltic Sea food chain

Gunilla Ejdung*

Department of Zoology and Department of Systems Ecology". Stockholm University, S-10691 Stockholm, Sweden

ABSTRACT: Behavioural responses of 2 Baltic benthic crustaceans to chemical substances from preda- tors were studied using infrared video-recording in the laboratory. This is the f~rststudy of behavioural responses to species-specific chemical substances in a 3-trophic-level food chain. Exposure to chemical substances from a predatory fish, the short-horned sculpin Myoxocephalusscorp~us(L.), ca.used the iso- pod Saduria entomon (L.)to remain buried in the sediment most of the time and decreased its foraging success on the amphipod Adonoporeia affinis (Lindstrom). M. aff~n~sdecreased its swimming activity when exposed to water from S. entomon feeding on M. affinls, whereas water from unfed S, entomon had no such effect.

KEY WORDS: Chemical cues . Three-trophic-level food chain - Monoporeia affinis . Saduria entomon Fish . Benthos Behaviour. Baltic Sea

INTRODUCTION McNamara & Houston 1992). To maximise fitness, for- agers should weigh potential energy gain against mor- In the aquatic environment, the use of chemical cues tality risk (Dill & Fraser 1984, Abrahams & Dill 1989). is probably universal (Dodson et al. 1994). Prey and Predation risk can be perceived through visual, predators can often discover and localise each other mechanical and chemical cues (Busdosh et al. 1982). through chemical cues, which may profoundly influ- Many aquatic invertebrates have small, poorly devel- ence their interactions (Sih 1986, Rittschof 1993, Abra- oped, non-image-forming eyes, sensitive mainly to hams 1994, Rochette et al. 1994). The life-history strat- changes in light intensity (Dodson et al. 1994), but egy (Crow1 & Covich 1990), behaviour (Folt & Goldman possess well-developed chemoreceptors (Laverack & 1981, Dodson et al. 1994, Duval et al. 1994), activity Ardill 1965, Pynnonen 1985, Larsson & Dodson 1993, pattern (Sih 1986, Holomuzki & Short 1988) and mor- Kaufman 1994). Chemical receptors and chemical cues phology (Appleton & Palmer 1988, Larsson & Dodson can be used in darkness and by animals that have poor 1993) of potential prey may be significantly affected by vision or do not see at all. Chemical cues may be mole- the presence of predators. Conventional optimal forag- cules large enough to be species-specific, such as pro- ing theory predicts that predators should maximise teins (Atema 1988). Concentration and/or composition their net rate of energy intake (Hughes 1980). Factors of the cue makes it possible to recognise a predator and influencing the rate of energetic acquisition, e.g. whether it is actively feeding, has recently fed or is energjr reserves and potential risks from predators, starving (Phillips 1978, Appelberg et al. 1993). Alarm have been taken into consideration (Sih 1982, Vadas et substances, originating from predator-mediated release al. 1994) and also included in models (Mange1 & Clark by injured conspecifics, reveal the presence of a preda- 1986, Gilliam & Fraser 1987, Burrows & Hughes 1991, tor (Appleton & Palmer 1988, Alexander & Covich 1991a, Hugie et al. 1991, Houtman & Dill 1994, Vadas et 'E-mail: [email protected] al. 1994) and may affect behaviour, growth rate, and "Present address morphology (Sih 1986, Appleton & Palmer 1988).

O Inter-Research 1998 Resale of full art~denot permitted 138 Mar Ecol Prog Ser

The question addressed here is whether chemical acclimatised almost without mortality to a gradual substances from predators influence the behaviour of 2 increase in salinity from 4 to 6.5 psu, the salinity in the Baltic benthic crustaceans. Thus, the aims of my exper- Asko area. S. entomon is a predator and a scavenger iments were to determine: (1) whether exposure to that possesses an array of feeding behaviours, and is chemical substances from a predatory fish, the short- reported to be mainly nocturnal (Westin & Aneer horned sculpin Myoxocephalus scorpius (L.), affected 1987).The eyes of S. entomon are small, with maximal the behaviour of the predatory isopod Saduria ento- sensitivity to green wavelengths, which dominate at mon (L.); (2) whether the rate of predation by S. the depths where this isopod lives. However, food is entomon on its natural prey, the amphipod Monoporeia located and recognised via chemoreceptors and chem- affinis (Lindstrom), changed in fish conditioned water; ical cues (Pynnonen 1985). S. entomon has 2 types of (3) whether exposure to the odour of starved S. ento- chemoreceptors, viz, distance chemoreceptors on the mon affected the activity and behaviour of M. affinis; first antennae and contact chemoreceptors on the and (4)whether M. affinis reacted to waterborne sub- mouth parts. Intact antennae are crucial for bilateral stances from S. entomon and its prey while the isopod antennular chemoreception (Pynnijnen 1985) of lulled, ate and digested individuals of M, affinis.The odours, such as those coming from dead fish. Small S. species chosen represent a naturally occurring 3- entomon avoid water from larger cannibalistic con- trophic-level system found in the species-poor Baltic specifics (Leonardsson 1991). benthic community. To my knowledge, this is the first In the Baltic, Saduria entomon is th.e main diet for study of the importance of behavioural responses to the short-horned sculpin Myoxocephalus scorpius species-specific chemicals in a 3-trophic-level food (Haahtela 1990) and is also eaten by the fourhorn chain. sculpin M. quadricornis (L.) (Westin 1970, Aneer 1975). The short-horned sculpins used in the experiments were caught with a gill net and kept in 60 1 containers MATERIAL AND METHODS at ca 7°C. Sediment and Monoporeia affinis were collected Study area, species studied, collection and treat- close to the laboratory, at 30 m depth, using a benthic ment of sediment and animals. This study was carried sled (Blomqvist & Lundgren 1996). The sediment was out in the northwestern Baltic proper at the Asko Lab- sieved through a 300 pm metal mesh net and kept cold oratory on the east coast of Sweden (58"49'N, prior to use. The amphipods were stored in aerated 1?"38'E). On the species-poor sub-thermocline ben- water in a thermostat controlled room (?"C), with a thic bottoms in this area, the amphipod Monoporeia daily 17 h light:? h dark cycle simulated with a dim affinisis one of the most abundant and productive spe- green light; the same light cycle as used in the experi- cies, with a natural abundance in 1981 to 1993 of 80 to ment. The day before the start of the experiment, indi- 2100 1 yr old (l+) M. affinis m-' at 27 m depth in the vidual M. affiniswere randomly picked in batches of 5 Asko area (station 6017 of the National Swedish Envi- and inspected under a stereomicroscope to ensure that ronmentaI Monitoring Program). M. affinis is a night- only intact amphipods were used. active surface-forager that mainly dwells in the upper The energy reserves of a predator often affect its for- 5 cm of the sediment (Hill & Elrngren 1987, Lopez & aging intensity (McNamara & Houston 1986). Even Elmgren 1989, Lindstrom et al. 1991). Late in the though Leonardsson (1991) found no difference in con- evening, the amphipods leave the bottom for excur- sumption rates for starved or fed Saduria entomon, the sions into the water column (Lindstrom & Lindstrom isopods in my experiments were deprived of food 2 d 1980).When they return to the bottom, they dig a new prior to the start of the experiment. S. entomon can sur- hole, in which they lie on the back. By moving the vive starvation for months with little mortality (author's pleopods, water is efficiently circulated into the bur- unpubl. obs.). Only non-gravid isopods with intact row (Lindstrom 1991). antennae were used. Abundances of the predatory isopod Saduria General experimental set-up. Square plastic entomon ranged from 0 to 110 ind. m-*during the same aquaria, placed in two ZOOl troughs (0.58 m') (Fig. l), period (Cederwall 1990, pers. comm.). In the late 1980s were used as containers. The aquaria had a sediment and early 1990s, S. entomon was easily caught in the area of 310 cm2 and l1 cm high walls, each of which study area, but by the summer of 1994, when this study had a 75 cm2 rectangular hole covered with a 0.2 mm was performed, sufficient numbers could not be mesh net, allowing water but not animals to pass obtained. S. entomon was therefore collected in the through. The sediment depth was 3.5 cm, just reaching Norrby archipelago, northern Bothnian Sea (63O30' N, the holes in the aquarium walls. Below the 100 1 19"501E),at a salinity of ca 4 psu. In the laboratory, the troughs, two 140 1 troughs (0.93 m'), one containing euryhaline (Lockwood & Croghan 1957) S, entornon sea water and one prepared water, were placed. Sea Ejdung: Behavioural responses to chemical cues of predation risk 139

Twelve video-recording cameras (Ikegami ICD- 42EAC) sensitive in the infrared region of the light spectrum were placed above the aquaria (Fig. 1). Lamps emitting sufficient infrared light (>B80 nm) for the registering cameras were used. The light sensitiv- ity of Monoporeia affinis declines sharply towards the red end of the spectrum (Donner 1971), as does that of Saduria entomon (Lindstrom et al. 1991), and neither species can detect infrared light (Donner & Lindstrom 1980, Lindstrom et al. 1991). Time-lapse recording started prior to the addition of S. entomon. A sequen- tial video-switcher activated the recording cameras in turn from camera 1 to 12 and then repeated the pro- cedure. Recording time was registered on the video- tape, and intervals between moving pictures as seen on the TV monitor were 2.2 or 4.1 S, respectively, for 24 h and 48 h long time-lapse recordings. It was not possible to quantify accurately the number of amphipods swimming at a given time, hence swim- ming activity was registered as present as soon as a single amphipod was seen swimming. As the record- ing time was registered on the videotape it was possi- ble to determine the duration of the different activities of the animals. When terminating the experiments, the sediment was sieved, and amphipods retained on a 500 pm mesh metal net were preserved in 4 % buffered formalin and stained with Rose Bengal. The length of the amphipods was measured on straightened out animals from the tip Fig. 1. Experimental set-up. Aquaria were connected to sea or of the rostrum to the end of the last urosome segment prepared water (lower trough) via a peristaltic pump. Video- with an image analyzing system (Zeiss, MOP video- cameras were placed above the aquaria. Infrared light emit- plan). Isopod length was measured from the anterior tors (to the left of the aquaria) made video-recording possible end of the head shield to the tip of the telson. in the dark Fish experiment. In order to test whether chemical substances from predatory fish influence the behav- water was pumped into the aquaria in one of the upper iour of Saduria entomon, and ultimately the survival of troughs, and prepared water into the aquaria in the its amphipod prey (Monoporeia affinis),the following 4 other upper trough. Water flow into each aquarium, treatments were set up: (1) S. entomon and M. affinis 0.8 0.1 1h-', was regulated with a multi-channel peri- in untreated sea water (8 aquaria), (2) S. entomon and staltic pump (Alitea, Stockholm, Sweden). The sea M. affinis in fish-treated water (8 aquaria), (3) controls water came from 16 m depth; it was filtered through with M. affinis alone in untreated sea water (3 sand (grain size 0.6 to 0.8 mm) and cooled (ca ?"C, aquaria), and (4) Ad. affinis in fish-treated water (3 salinity 6.5 psu) before reaching the troughs and was aquaria). This gave a total of 22 aquaria, 12 of which aerated once in the troughs. Cue water was prepared for each experiment. Table 1 Experimental set-up of the fish experiment. Fish were not fed during The fish, unfed isopod and fed isopod the experiment experiments were run consecutively, and the experimental equipment was Treatment No. of No. No. of S. No. of M. thoroughly cleaned prior to the start of aquaria filmed entomon affinis a new experiment to avoid contamina- aquarium-' aquarium-' tion between experiments. Using milk as a tracer, it was shown that the Sea H20 + S. entomon + M affinis 8 6 1 30 whole water volume of the experimen- Fish H20 + S. enton~on+ M. affjnis 8 6 1 3 0 Sea H20 + M. affinis 3 0 - 30 tal aquaria was reached by the incom- Fish H,O + M. affinis 3 0 - 30 ing fluid in less than 10 min. 140 Mar Ecol Prog Ser 165: 137-144, 1998

were video-recorded (6 each of treat- Table 2. Experimental set-up of the unfed isopod experiment. Isopods were ments 1 and 2) (Table 1). Video-record- not fed during the experiment ings were made in 48 h time-lapse mode for a total of 72 h. Treatment No. of No No. of M. Thirty adult Monoporeia affinis(F + SE, aquaria filmed affinis 7.8 + 0.2 mm long) were gently added to aquarium-' each box at the start of the experiment. Unfed-isopod-treated H20+ M. affinis 8 6 30 One Saduria entomon (30 + 1 mm) per Sea H20 + 1M. affjm-s 8 6 30 aquarium was added in treatments 1 and 2. Fish-treated water was prepared in one Table 3. Experimental set-up of the fed isopod experiment. Isopods were fed of the lower 140 1 troughs by keeping 3 amphipods during the experiment Myoxocephalus scorpius (total weight ca 1 kg) in Sea Water for 24 h prior to the start Treatment and during the entire fish experiment. Sea aquarium-' watertwice aand fish-treatedinto the troughs water were(Fig. refilledl). The \l Fed-isopod-treated H20 + M, affinis fish-treated water for refilling was pre- H,O + M. affir;is pared in 3 troughs, each of which held nothing but 1 short-horned sculpin (ca 0.3 kg) in 45 1 sea water. Unfed isopod experiment. The experiment was (= TT). When homogeneity of variances could not be designed to test whether Monoporeia affinisreacted to obtained through data transformation, the Mann- water which had contained unfed Saduria entomon. M. Whitney U-test was used. A paired t-test tested for affiniswere assigned at random to either of 2 treat- differences in the light/dark activity of Saduria ments: water from unfed isopods, or untreated sea entomon. Amphipod activity data was analysed u.sing water. Each treatment had 8 aquaria, 6 of which were 2-factor repeated measures ANOVA. Calculations video-recorded (for 22 h) as above (Table 2). Thirty M. based on a pilot study indicated that 8 replicates affinis(average size 7.8 * 0.2 mm) were added to each would be needed to achieve a power of 0.8 in order to aquarium. The unfed isopod-treated water was pre- detect a difference of at least 30% in amphipod sur- pared by keeping unfed isopods (37 specimens, total vival (Zar 1984). weight ca 24 g) in natural sea water in one of the lower 140 1 troughs (Fig. 1) for 48 h prior to and during the entire experiment. Water was not refilled. RESULTS Fed isopod experiment. To test if substances from Saduria entomon killing, eating and digesting Mono- Fish experiment poreia affinisaffected the behaviour of other M. affinis, fed-isopod-treated water, i.e. sea water containing 34 During the 72 h experimental period, Saduria isopods (mean body length ca 30 mm, total weight ca entomon spent only 0.8 + 0.3% (36 min) of its time at 22 g) and 340 amphipods (ca 7.7 + 0.2 mm) from a 140 1 the sediment surface in fish-treated water, but signifi- trough, or untreated sea water from another 140 1 cantly longer, 7.9 + 3.3% (340 min), in the sea water trough was added to aquaria, each containing 30 M. treatment (ANOVA, F,,9 = 13.8, p = 0.005). One S. affinis.The aquaria were video-recorded in 24 h time- entomon in the sea water treatment moulted and was lapse mode for 22 h (8 aquaria per treatment, 6 of excluded from the analysis. No differences in activity which were video-recorded) (Table 3). In the fed-iso- during the Iight and dark periods were found within pod-treated water trough, isopods were fed M, affinis the fish treatment (paired t-test, p > 0.05) or within 2 d prior to the experiment and during the entire the sea water treatment (paired t-test, p > 0.05) experiment. During this 3 d period, a total of 290 (Fig. 2). amphipods were consumed, i.e. ca 8 per isopod. Water Survival of Monoporeia affinisin the controls for the was not refilled. fish (29 * 1 specimens) and sea water (29 * 1 speci- Statistics. One-factor analysis of variance (ANOVA) mens) treatments and in the Saduria entomon with was used, except when variance was heterogeneous fish-treated water treatment (26 + 1 specimens) was according to Cochran's or Bartlett's test (balanced or significantly better than in the S. entomon with sea unbalanced treatments respectively). Significant re- water treatment (19 + 2 specimens) (ANOVA, F3,17= sults were followed by the Tukey test for unequal N 12.21, p = 0.0002; TT, p < 0.05) (Fig. 3). Ejdung: Behavioural responses to chemical cues of predation risk 141

Predator Predator Control Control fish sea fish sea Fish water Sea water water water water water

Fig. 2. Proportional activity of Saduria entomon in the fish Fig. 3. Number of Monoporeia affinis surviving in the pres- experiment Mean + standard error of the mean Black de- ence and absence (control) of Saduria entomon in the fish notes the dark period and white the light period experiment. 'Mean + standard error of the mean

treated water, swimming was reduced, occurring for only 16 k 4% of the total experimental time, while in sea water the corresponding figure was 72 * 6%. In both treatments, Monoporeia affinis was proportion- ally more active during the dark period (Fig. 5, Table 5).

DISCUSSION

Predation risk often affects prey behaviour (Alexan- der & Covich 1991b, Legault & Himmelman 1993), and Unfed Sea isopod water potential prey often shift into safer habitats (Dill 1987, water Lima & Dill 1990, Sih 1993, Jachner 1995) or spatially within habitats (Phillips 1977, Alexander & Covich Fig. 4. Monoporeia affinis proportional activity in the dark and light periods in the unfed isopod experiment. Mean + 1991b, Dix & Hamilton 1993) to avoid predation. Risk standard error of the mean. Black denotes the dark penod of predation usually reduces locomotory activity of and white the light period prey (Lima & Dill 1990, Sih 1993), which improves the chance of avoiding detection by the predator. Mono- Unfed isopod experiment poreia affinis and Saduria entomon were both less mobile in the presence of odour from their natural Amphipod survival was high, 97 ? 1 %, in both treat- predators, and both spent more time within the sedi- ments (ANOVA, FlSl4= 0.43, p = 0.52), with a similar ment. swimming activity, 82 * 1 % (of the total experimental The fish experiment indicates that Saduria entomon time) in sea water and 83 * 2 % in unfed-isopod-treated reacts to perceived predation risk with decreased water (Table 4); and for both treatments swimming was significantly more intense in the dark (Fig. 4, Table 4). All Saduria entomon survived. Table 4 Unfed isopod experiment. Two-factor repeated mea- sures ANOVA performed on Monoporeia affinis proportional activity during a light or dark period in unfed-isopod-treated Fed isopod experiment water or sea water (cue)

I Source of variauon df Amphipod- survival was 100 % in sea water and 96 + F 2% in fed-isopod-treated water (Mann-Whitney U- Cue 1 0.79 0.4159 test, p = 0.003, n = 16). All isopods survived. Amphipod ~,~h~/d~~k 1 54.94 0.0007 swimming activity was significantly affected by the Cue X light/dark 1 0.17 0 6961 origin of the added water (Table 5). In fed-isopod- 142 Mar Ecol Prog Ser 165: 137-144. 1998

Saduria entomon In sea water stayed mainly just below the sediment surface, with flicking antennae showing, thus Increasing the exposure of its chemical receptors to odour cues (Schmitt & Ache 1979). Short- horned sculpins are v~sualforagers with a die1 forag- ing cycle, being diurnal in winter and nocturnal in summer (Westin & Aneer 1987). The sculpins do not search for food within the sediment, but use an ambush technique (L. Westin pers. comm.). Foraging methods used by S. entomon include ambushing, or sit and wait, behaviour; sediment surface food search Fed Sea isopod water (fast active hunt, i.e. when the isopod swims or moves water on, or just below, the sediment surface with its body showing); and burrowing food search (slow active Fig. 5. Monoporeia affinis proportional activity in the dark and light periods in the fed isopod experiment. Mean + stan- hunt, used when food is searched for at depth in the dard error of the mean. Black denotes the dark period and sediment, with the body hidden in the sediment) white the light period (Green 1957, Pynnonen 1985, Ejdung & Bonsdorff 1992). The foraging methods used by S, entornor? Table 5. Fed isopod experiment. Two-factor repeated mea- change with exposure to fish-treated cue water, sug- sures ANOVA performed on Monoporeia affinis proportional gesting a perception of increased predation risk. activity in a light or dark period in fed-isopod-treated water or Although quick rushes over the sediment surface sea water (cue) might have provided S. entomon with food, the isopod seemed to search for food mainly within the sediment 1Source of variation df F when exposed to fish odour, video sequences some- Cue 1 184.50 0.00004 times showing movements of S. entomon within the Light/dark 1 62.04 0.00053 sediment. The change in behaviour, and use of a Cue X light/dark 1 1.19 0.32570 habitat spatially separated from that normally foraged in by short-horned sculpins, should lower encounter rates between short-horned, sculpins and S, entomon activity. When exposed to fish-treated cue water, the and increase isopod survival. However, predator activity of S. entomon at the sediment surface avoidance behaviours often lower food encounter decreased; Leonardsson (1991) found a similar reac- rates (Sih 1993), while energy continues to be used for tion for small S. entomon exposed to chemical cues maintenance and locomotion (Norberg 1977). Evi- from predatory larger conspecifics. In spite of the dently, S. entonlon searched for prey down in the sed- depressed activity of S. entomon, amphipods were still iment, and the number of prey consumed decreased, eaten, albeit at a slower rate than when fish odour was as often found when predatory fish are present (Holo- absent. muzki & Short 1988). When Saduria entomon was burrowed in the sedi- As sculpins in nature include amphipods in their diet ment, the antennae and head were occasionally seen, (Westin 1970), they directly affect amphipod survival. but the body was mostly hidden. In sea water, anten- This laboratory study of a benthic 3-trophic-level sys- nae were seen more frequently and for longer periods tem, with fish odour present during the whole expen- than in the fish-treated water. Once the antennae had ment, reflects a near distance predator-prey situation been withdrawn into the sediment, they were very dif- in the field. In the experiment, the presence of fish ficult to detect, except when exposed again at the odour had an indirect positive effect on amphipod sur- same, or nearly the same, spot where they had been vival, since the activity of the predatory isopod seen earlier. However, movement of a totally burrowed decreased. Saduria entomon in the experiment could S. entomon could sometimes be followed through only avoid the perceived predator by burrowing and ndgelike structures 'moving' over the sediment sur- decreasing its activity, but in nature another avoidance face, with some amphipods escaping from the sedi- behaviour, emigration, is possible (Sparrevik & Leon- ment just ahead of the moving isopod. When neither ardsson 1995), and probably important. parts of the body nor ridgelike structures were seen, Recently, the first steps in the characterization of the isopods remained undetected until appearing kairomones released by planktivorous fishes have again, at the sediment surface. No estimates of anten- been made (Loose et al. 1993, von Elert & Loose 1996). nal exposu.re or of behaviour within the sediment can The specifi.~substances released in my experiment are thus be presented. unknown. Additional research is needed to determine Ejdung: Behavioural responses to chemical cues of predation risk 143

the chemical composition of the substances, their nat- Alexander JE, Covich AP (1991a) Predator avoidance by the ural concentrations and their rate of degradation. freshwater snail Physella virgata in response to the cray- Recognition of chemical cues emitted by predators or fish Procambarus simulans. Oecologia 87:435-442 Alexander JE, Covich AP (1991b) Predation risk and avoid- injured conspecifics may increase prey survival, and ance behavior in two freshwater snails. Biol Bull (Woods many aquatic organisms possess this ability (Phillips Hole) 180:387-393 1978, Hugie et al. 1991, Covich et al. 1994, Duval et al. Aneer G (1975) Composition of food of the Baltic hernng (Clu- 1994). Large crustaceans obtain chemical information by pea harengus v membras L.), fourhorn sculpin (Myoxo- cephalus quadrjcornis L.) and eel-pout (Zoarces viviparus producing currents (Atema 1988), and Monoporeia affi- L.) from deep soft bottom trawling in the Asko-Landsort nis may receive a continuous flow of information on pre- area during two consecutive years. Merentutkimuslaitok- dation risk from chemical cues, which enter its burrow sen Julk 239.146-154 with the currents created by its beating pleopods. The Appelberg M, Soderback B, Odelstronl T (1993) Predator swimming activity of M. affinisdecreased drastically in detection and perception of predation risk in the crayfish Astacus astacus L. Nord J Freshwat Res 68:55-62 water with cues from Saduiia entomon fed M. affinis,in- Appleton RD, Palmer AR (1988) Waterborne stimull released dicating that M. affinisis able to evaluate the degree of by predatory crabs and damaged prey induce more preda- risk connected with the chemical information received. tor-resistent shells in marine gastropods. Proc Natl Acad The 'dietary history' of a predator often affects prey re- Sci USA 85:4387-4391 Atema J (1988) Distribution of chemical stimuli. In: Atema J, sponses (Duval et al. 1994). Lack of response to a non- Fay RR, Popper AN, Tavolga WN (eds) Sensory biology of foraging or starving predator has been reported also in aquatic animals. Springer-Verlag, New York, p 29-56 the sea urchins Strongylocentrotus purpuratus, in the Blomqvist S, Lundgren L (1996) A sled for sampling soft bot- freshwater snails Physella virgata and P. gyrina and the toms. Helgolander Meeresunters 50:453-456 cladoceran Daphnia galeata rnendotae (Phillips 1978, Burrows MT, Hughes RN (1991) Optimal foraging decisions by dogwhelks, Nucella Japillus (L.):influences of mortality Crowl & Covich 1990, Stirling 1995, Turner 1996). risk and rate-constrained digestion. Funct Ecol5:461-475 The Baltic benthic ecosystem has been considered as Busdosh M, Robilliard GA, Tarbox K. Beehler CL (1982) fairly simple, due to its low macro- and meiofaunal Chemoreception in an arctic amphipod crustacean: a field diversity (Elmgren 1978). Large areas in the Baltic are study. J Exp Mar Biol Ecol 62:261-269 Cederwall H (1990) Overvakning av mjukbottenfauna i covered by fine grained sediments, over which chemo- ~stersjonskustomrbde. Rapport frdn verksamheten 1989. reception works better than on coarse (ca 2 to 3 mm) SNV rapport 3796. ISBN 91-620-3?96X, ISSN 0282-7298 substrates (Weissburg & Zimmer-Faust 1993). Taking Covich AP, Crowl TA, Alexander JE Jr, Vaughn CC (1994) chemical predator-prey interactions into consideration Predator-avoidance responses in freshwater decapod-gas- will increase the complexity of interactions in this sys- tropod interactions mediated by chemical stimuli. J North Am Benthol Soc 13:283-290 tem. This laboratory study demonstrates that the Crowl TA, Covich AP (1990) Predator-induced life-history predator-prey interactions investigated are affected by shifts In a freshwater snail. Science 247.949-951 a variety of chemical cues from predators and prey. Dill LM (1987) Animal decision making and its ecological con- Further studies are required to evaluate better the sequences: the future of aquatic ecology and behaviour. Can J Zool 65:803-811 importance of such chemical cues in the field, and of Dill LM, Fraser AHG (1984) Risk of predation and the feeding indirect interactions between species caused by chem- behavior of juvenile coho salmon (Oncorhyncus kisutch). ical cues, in this community. Behav Ecol Sociobiol 16:65-71 Dix TL, Hamilton PV (1993) Chemically mediated escape Acknowledgements. I thank Barbro Soderlund for skilful behavior in the marsh periwinkle Littoraria irrorata Say. technical assistance in the field and laboratory, Car1 Andre J Exp Mar Biol Ecol 166:135-149 and Dennis Swaney for statistical d~scussions, B.-0 Jansson Dodson SI, Crowl TA, Peckarsky BL, Kats LB, Covich AP, for providing research facilities at the Asko Laboratory, the Culp JM (1994) Non-visual communicat~on in freshwater staff at the Asko Laboratory, and the Norrby Laboratory for benthos: an overview. J North Am Benthol Soc 13:268-282 providing isopods. Ragnar Elmgren, Christer Wiklund and Donner KO (1971) On vision in Pontoporeia affinis and anonymous reviewers gave critical comments on the manu- P. femorata (Crustacea, Amphipoda). Commentat Biol Soc script. This work was supported by grants from the Stockholm Sci Fenn 41:l-17 Centre for Marine Research, and Swedish Academy of Sci- Donner KO, Lindstrom M (1980) Sensitivity to light and clrca- ence (Hierta-Retzius foundation) to G.E., and by the Swedish dian activity of Pontoporeia affinjs (Crustacea, Amphi- Natural Science Research Council to R. Elmgren. poda) Ann Zool Fenn 17:203-212 Duval MA, Calzetta AM, Rittschof D (1994) Behav~oral responses of Littoraria irrorata (SAY) to waterborne odors. LITERATURE CITED J Chem Ecol20:3321-3334 Ejdung G, Bonsdorff E (1992) Predation on the bivalve Abrahams MV (1994) Risk of predation and its influence on Macoma balthica (L.) by the isopod Saduria entomon (L.): the relative competitive abilities of two species of fresh- laboratory and field experiments. Mar Ecol Prog Ser 88: water fishes. Can J Fish Aquat Sci 51.1629-1633 207-214 Abrahams MV. Dill LM (1989) A determination of the ener- Elmgren R (1978) Structure and dynamics of Baltic benthos getic equivalence of the risk of predation. Ecology 70: communities with particular reference to the relationship 999-1007 between macro- and meiofauna. Geler Meeresforsch 4.1-22 144 Mar Ecol Prog Ser 165: 137-144, 1998

Folt C, Goldman CR (1981) Allelopathy between zooplankton: Pontoporeia affinis and Pontoporeia femorata. Limnol a mechanism for interference competition. Science 213: Oceanogr 34:982-991 1133-1135 Mange1 M, Clark CW (1986) Towards a unif~edforaging the- Cilliam JF, Fraser DF (1987) Habitat selection under preda- ory. Ecology 5:1127-1138 tion hazard: test of a model with foraging minnows. Ecol- McNamara JM, Houston AI (1986) The common currency for ogy 68:1856-1862 behavioral decisions. Am Nat 127:358-378 Green J (1957) The feeding mechanism of Mesidotea ento- McNarnara JM, Houston AI (1992) Risk-sensitive foraging: mon (Linn.) (Crustacea: Isopoda). Proc Zool Soc Lond 129: a review of the theory. Bull Math Biol54:355-378 245-254 Norberg A (1977) An ecological theory on foraging time and Haahtela 1 (1990) What do Baltic studies tell us about the iso- energetics and choice of optimal food-searching method. pod Saduria entomon (L.)?Ann Zool Fenn 27:269-278 J Anim Ecol46:511-529 HLU C, Elmgren R (1.987)Vertical distribution in the sediment Phillips DW (1977) Avoidance and escape responses of the in the CO-occurringbenhc amphipods Pontoporeia affinis gastropod mollusc Olivella biplicata (Sowerby) to preda- and P. femorata. Oikos 49:221-229 tory asteroids. J Exp Mar Biol Ecol 28:77-86 Holomuzki JR, Short TM (1988) Habltat use and fish avoid- Phillips DW (1978) Chemical mediation of Invertebrate defen- ance behaviors by the stream-dwelling isopod Lirceus slve behaviors and the abllity to distinguish between for- fontinalis. Oikos 52:79-86 aging and inactive predators. Mar Biol 49:237-243 Houtman R, Dill LM (1994) The influence of substrate color on Pynnonen K (1985) The structure of long distance (antennular) the alarm response of tidepool sculpins (Oligocottus macu- chemoreceptors in Saduria entomon (L.), Isopoda, and their losus, Pisces, Cottidae). Ethology 96:147-154 role in feeding behaviour. Annl Zool Fenn 221423-432 Hughes RN (1980) Optimal foraging theory in the marine con- Rittschof D (1993) Body odors and neutral-basic peptide mim- text. Oreanogr Mar Biol Annu Rev 18:423-481 ics: -. review of responses by marii~eorganisms. Am Zoo! Hugie DM, Thuringer PL, Smith RJ (1991) The response of the 33:487-493 tidepool sculpin, OLigocottus maculosus, to chemical stim- Rochette R, Hamel JF, Himrnelman JH (1994) Foraging strat- uli from injured conspecifics, alarm signalling in the Cotti- egy of the asteroid Leptasteriaspolaris: role of prey odors, dae (Pisces). Ethology 89 322-334 current and feeding status. Mar Ecol Prog Ser 106:93-100 Jachner A (1995) Chemically-induced hahitat shifts in hl~ak Srhrrli!! RC, Ache SW (!9?9) n!fac!inr. respnr.ses cf 2 deca- (Nburnus albumus L.).Arch Hydrobiol 133171-79 pod crustacean are enhanced by flicking. Science 205: Kaufman RS (1994) Structure and function of chemoreceptors 204-206 in scavenging lysianassoid amphipods. J Crustac Biol 14: Slh A (1982) Foraging strategies and the avoidance of preda- 54-71 tion by an aquatic insect, Notonecta hoffmanni. Ecology Larsson P, Dodson S (1993) Invited review. Chemical commu- 631786-796 nication in planktonic animals. Arch Hydrobiol 129: Sih A (1986) Antipredator responses and the perception of 129-155 danger by mosquito larvae. Ecology 67:434-441 Laverack MS, Ardill DJ (1965) The innervation of the aes- Sih A (1993) Effects of ecological interactions on forager diets: thetasc hairs of Panulirus argus. Q J Microsc Sci 106: composition, predation risk, parasitism and prey behav- 45-60 iour. In: Hughes RN (ed) Diet selection: an interdiscipli- Legault C, Himmelman JH (1993) Relation between escape nary approach to foraging behaviour. Blackwell, Oxford, behaviour of benthic marine invertebrates and the risk of p 182-211 predation. J Exp Mar Btol Ecol 170:55-74 Sparrevik E, Leonardsson K (1995) Effects of large Saduna Leonardsson K (1991) Effects of cannibalism and alternative entomon (Isopoda) on spatial distribution of their small S. prey on population dynamics of Saduria entomon entomon and Monoporela affinls (Amphipoda) prey. (Isopoda). Ecology 72~1273-1285 Oecologia 1011177-184 Lima SL, Dill LM (1990) Behavioral decisions made under the Stirling G (1995) Daphr~iabehaviour as a bioassay of fish risk of predation: a review and prospectus. Can J Zool 68: presence or predation. Funct Ecol8:778-784 619-640 Turner AM (1996) Freshwater snails alter habitat use in Lindstrom M (1991) Factors affecting the horizontal migration response to predation. Anim Behav 51:747-756 of the amphipod Pontoporeia affinis Lindstrom. I. Record- Vadas RLS, Burrows MT, Hughes RN (1994) Foraging strate- ing method and response to water currents. J Exp Mar Biol gies of dogwhelks, Nucella lapiUus (L.):interacting effects ECO~150:149-162 of age, diet, and chemical cues to the threat of predation. Lindstrom M, Fortelius W, Meyer-Rochow VB (1991) Expo- Oecologia 100:439-450 sure to bright light has little effect on eye sensitivity and von Elert E, Loose CJ (1996) Predator-induced diel vertical ultrastructure of Saduria entomon (Crustacea, Isopoda, migration in Daphnia: enrichment and preliminary chem- Valvifera). Zool Sci 8.653-653 ical characterization of a ka~rornone exuded by fish. Lindstrom M,kndstrom A (1980) Swimming activity of Ponto- J Chem Ecol22:885-895 poreia affinis (Crustacea, Amphipodal-seasonal varia- bVe1ssburg MJ, Zirnmer-Faust RK (1993) Life and death in tions and usefulness for environmental stuhes. Ann Zool moving fluids: hydrod.ynamic effects on chemosensory- Fenn 17:213-220 mediated predation. Ecology 741428-1443 Lockwood APM, Croghan PC (1957) The chloride regulation Westin L (1970) The food ecology and the annual food cycle in of the braclush and fresh-water races of Mesidotea ento- the Baltic population of fourhorn sculpin, Myoxocephalus mon (L.). J Exp Biol 34:253-258 quadricornis (L.).Pisces. Rep Inst Freshtvat Res Drottning- Loose CJ, von Elert E. Dawidowicz P (1993) Chemically- holm 50:168-210 induced diel vertical migration in Daphnia: a new bio- Westin L, Aneer G (1987) Locomotor activity patterns of nine- assay for kairomones exuded by fish. Arch Hydrobiol 126: teen fish and five crustacean species from the Baltic Sea. 329-337 Environ Biol Fishes 20:49-65 Lopez G, Elmgren R (1989) Feeding depths and organic Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall, absorption for the deposit-feeding benthic amphipods Englewood Chffs, NJ

Editorial responsibility. Otto Kinne (Editor), Submitted: October 6, 1997; Accepted- February 23, 1998 Oldendorf/Luhe, Germany Proofs received from author(s). Apnl20, 1998